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Thoracic Imaging |
1 From the Department of Radiology and the Medical Research Group (EA2682), University Center Hospital Calmette, Blvd Jules Leclerc, Lille 59037, France (I.M., M.R.J., J.R.); and the Environmental and Occupational Health and Ergonomics Research Center, University of Lille (A.S., C.B., J.L.E.), France. Received June 30, 2000; revision requested August 8; revision received August 31; accepted September 19. Address correspondence to M.R.J. (e-mail: mremy-jardin@chru-lille.fr).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Two hundred fifty volunteers (133 women, 117 men; mean age, 39 years), including 144 smokers, 47 ex-smokers, and 59 nonsmokers, prospectively underwent inspiratory and expiratory high-spatial-resolution computed tomography (CT) and pulmonary function tests (PFTs). The frequency and characteristics of air trapping were evaluated according to the population’s smoking habits and PFT results.
RESULTS: The overall frequency of air trapping was 62% (155 of 250 subjects). Lobular air trapping was depicted in 117 (47%) of 250 subjects, without significant differences among smokers (n = 91), ex-smokers (n = 33), and nonsmokers (n = 31) (P = .118). Segmental and lobar air trapping (38 [15%] of 250) were more frequent among smokers (24 [26%] of 91) and ex-smokers (nine [27%] of 33) (P < .001). No relationship was found between air trapping and functional indexes of small-airway disease when the CT pattern of air trapping was considered. The strongest relationship between CT abnormalities and functional alterations at the small-airways level was between inspiratory CT features of bronchiolitis: ground-glass opacity, ill-defined micronodules, bronchiolectasis, and air flow at low lung volumes.
CONCLUSION: Whereas a significant relationship was observed between segmental and lobar air trapping and cigarette consumption, lobular air trapping was not found to reflect functional impairment at the small-airways level.
Index terms: Bronchiolitis, 60.2191, 60.269 • Computed tomography (CT), high-resolution, 60.12111, 60.12118 • Lung, abnormalities, 60.2191, 60.269 • Lung, function • Lung, air trapping, 60.29 • Small airways disease, 60.2191, 60.269
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Patients were clinically evaluated by means of a standardized questionnaire that was modified from one used by the British Occupational Hygiene Society Committee on Hygiene Standards (7) and included questions about the presence of any isolated respiratory symptom (eg, cough, sputum production [both recorded as occurring in the morning or all day], dyspnea, or wheezing) or chronic bronchitis. Chronic bronchitis was diagnosed by using the criteria defined by the American Thoracic Society (8). For each subject, the gathered clinical information included age, height, weight, smoking history including cigarette consumption (evaluated in pack years), and the duration of smoking cessation (if any), expressed in years.
Subjects were included in the study on the basis of (a) a knowledge of their medical background (thus excluding those who had previously undergone chest surgery; had pleural disease or a previous respiratory illness, especially bronchiolitis of any origin in previous years or infancy; or had known exposure to environmental and/or occupational pollutants); (b) knowledge of their smoking history (quantitative estimates of the number of cigarettes consumed [ie, number of pack years] and duration of cigarette consumption [ie, total lifetime cigarette consumption]; and (c) the absence of respiratory complaints. The last criterion included subjects with truly normal clinical evaluation results (no respiratory symptoms) or minimal respiratory symptoms; these symptoms varied from isolated symptoms (cough, sputum production, dyspnea after strenuous activity) to mild chronic bronchitis, were detected only by means of a clinical questionnaire, and were commonly considered to be normal among smokers.
We systematically excluded subjects who had severe dyspnea (grade 2 or 3) or any form of chronic bronchitis complicated by respiratory infections and/or right ventricular failure. Subjects also were excluded from the final study group if evidence of extensive intrathoracic abnormalities (eg, parenchymal scars, infiltrates of unknown origin) was seen at CT or if they did not complete all phases of the study.
The final study group comprised 250 subjects: 133 women and 117 men who ranged in age from 20 to 59 years (mean age, 39 years). The group was separated into current smokers (smoked regularly for more than 5 years; n = 144); ex-smokers (had not smoked for more than 2 years; n = 47), and nonsmokers (n = 59). PFT was performed immediately after clinical evaluation; chest radiographs and chest CT scans were obtained within 3 weeks after inclusion in the study.
Pulmonary Function Testing
PFT was performed to obtain flow-volume curves. Maximum expiratory flow-volume curves were obtained by measuring flow with a pneumotachygraph (Spiroanalyser ST-300; Fukuda, Nagareyama, Japan). Calibration of the pneumotachygraph, maneuvers performed, and selection of curves met the American Thoracic Society guidelines (9,10). The following parameters were evaluated: forced vital capacity (FVC); forced expiratory volume in 1 second (FEV1); ratio of FEV1 to FVC (FEV1/FVC); and maximal expiratory flow (MEF) at 75%, 50%, and 25% of FVC (MEF 75, MEF 50, and MEF 25, respectively). All spirometric values were expressed as a ratio of measured to predicted values. Prediction equations were previously provided by Knudson et al (11,12) for all parameters.
Closing volume (CV), which reflects the closure of dependent airways, was measured by performing single-breath nitrogen tests, by using the PFDX unit (Medical Graphics, St. Paul, Minn). While seated, subjects were asked first to breathe quietly, then to expire slowly and deeply until they reached their residual volume. This maneuver was followed by a deep and slow inspiration of oxygen, then by a deep expiration at a flow rate as near as possible to .5 L/sec, during which expiratory nitrogen was analyzed and plotted against volume. Computed results were the CV alone; the CV related to vital capacity (VC), that is, CV/VC; and the slope of the alveolar plateau (phase III), with the last parameter reflecting changes in small-airway disease in the presence of an upward-sloping plateau. The procedure was repeated, with a minimum interval of 10 minutes, to ensure good reproducibility, namely values differing by less than 5%. Test results were expressed as a ratio of measured to predicted ratios; predicted values were given by Buist and Ross (13).
Functional residual capacity was determined by performing body plethysmography with a Jaeger apparatus (Master Lab, Wursbourg, Germany). By using the ratio of pressure and volume of the box, functional residual capacity was computed according to the American Thoracic Society’s recommendations. Test results were expressed as measured to predicted value ratios; predicted values were provided by Quanjer et al (14).
CT Evaluation
During the inclusion period, CT evaluation was performed successively with Somatom Plus and Somatom Plus A4 CT units (Siemens, Erlangen, Germany). With the Somatom Plus scanner, 1-mm-thick sections, a 350-mm field of view, a 512 x 512 reconstruction matrix, 137 kV, 275 mA, and a 1-second scanning time were used; with the Somatom Plus A4 scanner, 140 kV, 206 mA, and a .75-second scanning time were used. The examinations consisted of obtaining end-inspiratory and end-expiratory thin-section CT scans; the former were obtained at 10-mm intervals from the lung apices to below the costophrenic angles, and the latter were obtained at five selected levels: 2 cm above the aortic arch, the aortic arch, the tracheal carina, 1 cm below the carina, and 2 cm above the diaphragm. All images were reconstructed by using a high-spatial-frequency algorithm. All patients underwent scanning in the supine position. Lung images, including inspiratory and expiratory scans, were obtained with the same window settings: a level of 1,600 HU and a center of -600 HU.
Without knowledge of participant smoking habits, two experienced chest radiologists (I.M., M.R.J.) independently viewed the images from each CT study in random order, interpreting first the expiratory and then the inspiratory CT scans of each patient. This order was chosen to avoid any bias in the interpretation of expiratory scans from the identification of inspiratory CT features of small-airway disease. In cases of discordant analysis, the final interpretation was reached with consensus.
On expiratory CT scans, the pattern, extent, and distribution of air trapping were visually analyzed. Air trapping was classified as lobular when it was composed of small areas of hypoattenuation that corresponded to fewer than three adjacent secondary pulmonary lobules, as segmental when an area of hypoattenuation between three adjacent secondary pulmonary lobules and a pulmonary segment was depicted, and as lobar when an area of hypoattenuation larger than a pulmonary segment was observed. When several patterns of air trapping were concomitantly depicted, the most severe pattern was systematically considered. The extent of air trapping was determined by calculating the mean percentage of cross-sectional area affected by hypoattenuation on the five expiratory CT scans obtained per patient. This mean percentage included three main categories: air trapping affecting less than 25%, 25%–75%, or greater than 75% of the lung surface. Vertical, anteroposterior, and uni- or bilateral distribution of air trapping were included in the interpretation of expiratory CT scans. On inspiratory CT scans, CT features related to cigarette smoking were systematically searched for, namely ill-defined micronodules, ground-glass opacity, emphysema, bronchial wall thickening, and bronchiectasis. In addition, the presence of dependent lung opacity and heterogeneous lung attenuation (defined by areas of hypoattenuation intermingled with normal lung) was coded.
Statistical Analyses
Statistical analyses were performed with SAS software (SAS, Cary, NC) and a microcomputer (XPS 166; Dell, Austin, Tex). Means, SDs, and frequencies were calculated. As is common in pulmonary function measurement, all parameters were treated as independent values because they indicated different aspects of lung health status. Quantitative data were compared by performing one-way analysis of variance (general linear model procedure); when these test results were significant, the Tukey multiple comparison test was performed. Analysis of contingency tables was performed with the 
2 or Fisher exact test when table cells had expected values of less than five. Multiple stepwise logistic regression analysis by means of forward selection was performed to examine the independent association between several predictor variables with regard to the presence of pulmonary function parameter abnormalities. Predictor variables incorporated into the multivariate logistic model included CT scan abnormalities that were coded in dichotomous variables. The pool of independent variables included ill-defined micronodules, areas of ground-glass opacity, emphysema, bronchial wall thickening, heterogeneous lung attenuation, and air trapping on the expiratory scans. Agreements between the two observers for CT findings were assessed by using the 
statistic.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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> 0.80 in all instances).
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A significantly higher frequency of segmental air trapping was found in subjects with abnormal inspiratory thin-section CT scans, as compared with subjects with normal inspiratory thin-section CT scans (24 [19%] of 125 vs 12 [10%] of 125, respectively; P < .05). Three inspiratory CT abnormalities were observed with a significantly higher frequency among the 155 subjects who had air trapping on expiratory scans, as compared with the 95 subjects who did not: ill-defined micronodules (39 [25%] of 155 subjects vs 13 [14%] of 95 subjects, respectively; P < .05), dependent lung density (19 [12%] of 155 subjects vs four [4%] of 95 subjects, respectively; P < .05), and heterogeneous lung attenuation (10 [6%] of 155 subjects vs one [1%] of 95 subjects, respectively; P < .05). Among smokers (n = 144), ill-defined micronodules on inspiratory thin-section CT scans were seen with a significantly higher frequency when air trapping was present on expiratory scans (38 [42%] of 91 subjects with air trapping at expiratory CT vs 11 [21%] of 53 subjects without air trapping at expiratory CT; P < .05).
No significant difference was found between the mean values of functional parameters in subjects who had air trapping, as compared with subjects who did not have air trapping. In accordance with criteria used by Knudson et al (11,12), three subgroups of functional profiles were defined: (a) subjects who had normal PFT results (n = 214 [86%]), (b) subjects who had an obstructive pattern (n = 28 [11%]), and (c) subjects who had small-airway disease (n = 7 [3%]). No relationship was found between CT findings at expiration and the functional categories previously defined.
Only seven subjects had functional parameters suggestive of small-airway disease. Five functional parameters suggestive of small-airway disease, expressed as a ratio of measured to predicted values, were defined as follows: (a) the slope of the alveolar plateau (phase III) greater than 1.4 of predicted values, (b) the closing volume (in percentage of vital capacity) greater than 1.4 of predicted values; (c) an MEF 50 of less than 0.60 of predicted values; (d) an MEF 25–75 of less than 0.60 of predicted values, and (e) a residual volume greater than 1.20 of predicted values. No relationship was found between CT findings at expiration and functional indexes of small-airway disease (Table 5). At stepwise regression analysis, the major morphologic determinants of small-airway disease were inspiratory CT findings (Table 6) (Figs 4, 5).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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In three studies in which ventilation abnormalities in obstructive airways disorders were investigated (4,15,16), healthy subjects were examined as a control group and underwent scanning at expiration. Whereas air trapping was identified in each of the 28 healthy nonsmokers in the study by Park et al (4), none of the six healthy subjects evaluated by Suga et al (15) had focal areas of hypoattenuation. Such results may be due to differences in the CT protocols used for each investigation on the basis of serial sequential expiratory thin-section CT scanning in the study by Park et al (4) and in the present study and on dynamic expiratory spiral CT performed by Suga et al (15), with subsequent analysis of the same anatomic level during two to three respiratory cycles. In addition, it should be noted that no data were available on the smoking habits of the six healthy subjects who underwent scanning in the study by Suga et al (15). In the third study we are aware of in which healthy subjects were evaluated as control groups (16), no air trapping was reported on the expiratory CT scans of 10 healthy nonsmokers. These results may be explained by the study design, in which areas of decreased attenuation in fewer than five individual secondary pulmonary lobules per lung were considered to be physiologic features.
To our knowledge, ours is the first study to include a systematic analysis of the CT patterns of air trapping in healthy volunteers. Lobular air trapping was the most frequently depicted and was observed in 117 (47%) of the 250 enrolled subjects. This pattern consisted of small areas of hypoattenuation of fewer than three adjacent secondary pulmonary lobules. Several findings suggest that this CT feature does not reflect small-airway disease. First, there was no significant difference in the frequency of lobular air trapping among smokers, ex-smokers, and nonsmokers—74% (67 of 91 subjects), 73% (24 of 33 subjects), and 84% (26 of 31 subjects), respectively. Second, we failed to demonstrate any relationship between the presence of lobular air trapping and PFT abnormalities, with consideration of the functional profiles of the study population or the functional indexes of small-airway disease. According to the results of stepwise regression analysis, the major morphologic determinants of small-airway disease in our population were inspiratory CT findings. In addition to bronchial wall thickening and bronchiolectasis, ill-defined micronodules and areas of ground-glass opacity are known to reflect respiratory bronchiolitis and surrounding macrophage alveolitis, which are two typical pathologic features of smoker’s bronchiolitis (17).
Despite the lack of significant relationships between air trapping and alterations of PFT results, our results suggest that segmental and lobar air trapping are CT patterns that are highly suggestive of small-airway disease. First, these patterns of air trapping were observed with a significantly higher frequency among smokers and ex-smokers, as compared with nonsmokers. Second, a higher frequency of segmental air trapping was observed in the subgroup of heavy smokers, as compared with mild smokers, and the pattern of lobar air trapping was found exclusively in heavy smokers. In addition, these features were observed with a significantly higher frequency in subjects who had inspiratory CT features of smoker’s lung. One might question the presence of segmental air trapping in nonsmokers. It should be noted that mild clinical symptoms also were depicted in this subgroup; this finding suggests either concomitant adverse effects of air pollution in this population of urban dwellers or, more likely, an unknown previous history of respiratory disease; thus, the possibility that these volunteers are not truly representative of a healthy population is raised. We did not find any relationship between segmental and lobar air trapping and PFT result abnormalities.
Similar findings have been recently reported by Lee et al (6), who observed that PFT results were within normal ranges in all participants, regardless of the presence of air trapping. As previously emphasized by Park et al (4), this apparent discrepancy may be due to the possibility of identifying focal abnormalities on CT scans, whereas the spirometric measurements provide a more global measure of lung function. Moreover, the CT protocol was limited to five expiratory thin-section CT scans that were obtained after deep inspiration. Another potential explanation concerns the major differences in the subjects’ position for each investigation: seated for PFT and supine for CT. Therefore, detection of large areas of hypoattenuation at expiration in the absence of functional abnormalities suggests that CT is a more sensitive method for detecting small-airway abnormalities than is PFT. This supports previous observations, according to which expiratory CT should complement the basic search for small-airway disease (6,18).
Our study had several limitations. Although all subjects were highly cooperative, we did not perform spirometrically gated CT and thus did not control the degree of each expiratory maneuver. Moreover, expiratory CT scans were obtained after deep expiration. Because respiratory status varies remarkably among subjects, forced maneuvers may lead to greater variability in respiratory change in lung attenuation, as emphasized by Suga et al (15). Another limitation was the visual assessment of the extent of air trapping; it could have been more precisely delineated by means of superimposed grids on high-spatial-resolution CT scans to count the number of squares that contained lung tissue of decreased attenuation. Moreover, it should be emphasized that almost 60% of the volunteers enrolled in the present study were smokers; this high proportion may have interfered with the overall CT findings.
In conclusion, lobular air trapping occurred in 47% of healthy volunteers and was related to neither the participants’ smoking habits nor the functional indexes of small-airway disease. Segmental and lobar air trapping had significant relationships with heavy cigarette consumption and should remain CT markers of small-airway disease. Our results suggest that the pattern and not simply the presence of air trapping should be analyzed on expiratory CT scans whenever CT features of small-airway disease must be detected.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, M.R.J., J.R.; study concepts and design, M.R.J., J.R.; definition of intellectual content, M.R.J.; literature research, M.R.J., J.R.; clinical studies, A.S., C.B., J.L.E.; data acquisition, M.R.J., J.R.; data analysis, M.R.J., J.R., I.M.; statistical analysis, J.L.E.; manuscript preparation and editing, M.R.J.; manuscript review, J.R.
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